Abstract

Plant infection by pathogenic fungi involves the differentiation of appressoria, specialized infection structures, initiated by fungal sensing and responding to plant surface signals. How plant fungal pathogens control infection-related morphogenesis in response to plant-derived signals has been unclear. Here we showed that the morphogenesis-related NDR kinase pathway (MOR) of the cucumber anthracnose fungus Colletotrichum orbiculare is crucial for appressorium development following perception of plant-derived signals. By screening of random insertional mutants, we identified that the MOR element CoPag1 (Perish-in-the-absence-of-GYP1) is a key component of the plant-derived signaling pathway involved in appressorium morphogenesis. Constitutive activation of the NDR kinase CoCbk1 (Cell-wall-biosynthesis-kinase-1) complemented copag1 defects. Furthermore, copag1 deletion impaired CoCbk1 phosphorylation, suggesting that CoPag1 functions via CoCbk1 activation. Searching for the plant signals that contribute to appressorium induction via MOR, we found that the cutin monomer n-octadecanal, degraded from the host cuticle by conidial esterases, functions as a signal molecule for appressorium development. Genome-wide transcriptional profiling during appressorium development revealed that MOR is responsible for the expression of a subset of the plant-signal-induced genes with potential roles in pathogenicity. Thus, MOR of C. orbiculare has crucial roles in regulating appressorium development and pathogenesis by communicating with plant-derived signals.

Highlights

  • We demonstrate that the widely conserved morphogenesis-related NDR kinase pathway (MOR) of C. orbiculare regulates infection structure development triggered by plant-derived signals and involves in pathogenesis

  • We show that the signal molecule for appressorium induction via MOR is the cutin monomer n-octadecanal degraded from the host plant cuticle by conidial surface esterases

  • We examined whether the reintroduction of CoKEL2 into those mutants restored normal appressorium formation on artificial substrates to isolate mutants that have defects in the CoKEL2-independent and the plant-derived signaling pathways for appressorium formation

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Summary

Introduction

In many plant pathogenic fungi including Colletotrichum species, adhesion to the plant surface is the first step to initiate the infection process [3]. Previous studies have revealed that physical signals including hardness and hydrophobicity stimulate conidium germination and appressorium formation Besides such physical stimuli, chemical signals such as leaf waxes and cutin monomers induce appressorium formation in several plant pathogenic fungi. Analysis of the genome-wide expression profiles of C. higginsianum revealed that appressoria formed in vitro are morphologically indistinguishable from those in planta, their transcriptomes are substantially different. This indicates that these specialized cells are highly responsive to plant-derived signals that are perceived before penetration [2]

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